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Distribution of axon diameters in cortical white matter: an electron-microscopic study on three human brains and a macaque.

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Liewald, Daniel, Miller, Robert, Logothetis, Nikos, Wagner, Hans-Joachim, Schüz, Almut·2014·Biological Cybernetics
DOI 10.1007/s00422-014-0626-2PMC PMC4228120
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Abstract

The aim of this study was to obtain information on the axonal diameters of cortico-cortical fibres in the human brain, connecting distant regions of the same hemisphere via the white matter. Samples for electron microscopy were taken from the region of the superior longitudinal fascicle and from the transitional white matter between temporal and frontal lobe where the uncinate and inferior occipitofrontal fascicle merge. We measured the inner diameter of cross sections of myelinated axons. For comparison with data from the literature on the human corpus callosum, we also took samples from that region. For comparison with well-fixed material, we also included samples from corresponding regions of a monkey brain (Macaca mulatta). Fibre diameters in human brains ranged from 0.16 to 9 μm. Distributions of diameters were similar in the three systems of cortico-cortical fibres investigated, both in humans and the monkey, with most of the average values below 1 μm diameter and a small population of much thicker fibres. Within individual human brains, the averages were larger in the superior longitudinal fascicle than in the transitional zone between temporal and frontal lobe. An asymmetry between left and right could be found in one of the human brains, as well as in the monkey brain. A correlation was also found between the thickness of the myelin sheath and the inner axon diameter for axons whose calibre was greater than about 0.6 μm. The results are compared to white matter data in other mammals and are discussed with respect to conduction velocity, brain size, cognition, as well as diffusion weighted imaging studies.

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Figures

Fig. 1 Left hemisphere of brain 3, indicating the course of the two macroscopic sections by stippled lines
Fig. 1 Left hemisphere of brain 3, indicating the course of the two macroscopic sections by stippled linesCC BY · PubMed Central
Fig. 2 Brain 3, location of the three samples taken from the corpus callosum of brains 2 and 3
Fig. 2 Brain 3, location of the three samples taken from the corpus callosum of brains 2 and 3CC BY · PubMed Central
Fig. 3 Coronal section through the left hemisphere of brain 2 (see Fig. 1), rostral side of the posterior part of the hemisphere. It shows the location of the sample cut out for further investigation. One edge of the sample has been chamfered to facilitate orientation of semi-thin sections
Fig. 3 Coronal section through the left hemisphere of brain 2 (see Fig. 1), rostral side of the posterior part of the hemisphere. It shows the location of the sample cut out for further investigation. One edge of the sample has been chamfered to facilitate orientation of semi-thin sectionsCC BY · PubMed Central
Fig. 4 Electron micrographs from the superior longitudinal fascicle of human brain 2, illustrating the selection of profiles. The broken lines indicate the borders of the evaluated area in each electron micrograph. Profiles extending over the upper and left borders are discarded. The black lines within the profiles show how their diameters have been measured. Bars 5 μm
Fig. 4 Electron micrographs from the superior longitudinal fascicle of human brain 2, illustrating the selection of profiles. The broken lines indicate the borders of the evaluated area in each electron micrograph. Profiles extending over the upper and left borders are discarded. The black lines within the profiles show how their diameters have been measured. Bars 5 μmCC BY · PubMed Central
Fig. 5 Electron micrographs from human brain 1, a from the superior longitudinal fascicle, b from the uncinate/inferior occipitofrontal fascicle. Left left hemisphere, right right hemisphere. Bars 5 μm
Fig. 5 Electron micrographs from human brain 1, a from the superior longitudinal fascicle, b from the uncinate/inferior occipitofrontal fascicle. Left left hemisphere, right right hemisphere. Bars 5 μmCC BY · PubMed Central
Fig. 6 Electron micrographs from the region of the superior longitudinal fascicle of the macaque brain (M. mulatta). a and b show regions where all fibres run orthogonally to the frontal sections, c and d show a neighbouring region with fibres running also in other directions. This region was not included in the measurements, but is shown here for illustrating different aspects of the cortical white matter. Bars 5 μm
Fig. 6 Electron micrographs from the region of the superior longitudinal fascicle of the macaque brain (M. mulatta). a and b show regions where all fibres run orthogonally to the frontal sections, c and d show a neighbouring region with fibres running also in other directions. This region was not included in the measurements, but is shown here for illustrating different aspects of the cortical white matter. Bars 5 μmCC BY · PubMed Central
Fig. 7 Electron micrograph from the corpus callosum of the macaque, showing the large range of diameters. Bar 5 μm
Fig. 7 Electron micrograph from the corpus callosum of the macaque, showing the large range of diameters. Bar 5 μmCC BY · PubMed Central
Fig. 8 Frequency distribution of the diameters of myelinated axons in the superior longitudinal fascicle of the three human brains in the left and right hemisphere
Fig. 8 Frequency distribution of the diameters of myelinated axons in the superior longitudinal fascicle of the three human brains in the left and right hemisphereCC BY · PubMed Central
Fig. 9 Frequency distribution in the uncinate/inferior occipitofrontal fascicle in the three human brains
Fig. 9 Frequency distribution in the uncinate/inferior occipitofrontal fascicle in the three human brainsCC BY · PubMed Central
Fig. 10 a and b Frequency distribution of the diameters of myelinated axons in three different locations of the corpus callosum in human brains 2 and 3 (CC1 genu, CC2 truncus, CC3 splenium). The largest value in human brain 3 is 5.13 μm and is not contained anymore in the diagram. c Axon diameters from the truncus of the corpus callosum of the rhesus monkey
Fig. 10 a and b Frequency distribution of the diameters of myelinated axons in three different locations of the corpus callosum in human brains 2 and 3 (CC1 genu, CC2 truncus, CC3 splenium). The largest value in human brain 3 is 5.13 μm and is not contained anymore in the diagram. c Axon diameters from the truncus of the corpus callosum of the rhesus monkeyCC BY · PubMed Central
Fig. 11 Frequency distribution of the diameters of myelinated axons in the rhesus monkey. a region of the superior longitudinal fascicle, right hemisphere only, b region of the uncinate/inferior occipitofrontal fascicle, both hemispheres
Fig. 11 Frequency distribution of the diameters of myelinated axons in the rhesus monkey. a region of the superior longitudinal fascicle, right hemisphere only, b region of the uncinate/inferior occipitofrontal fascicle, both hemispheresCC BY · PubMed Central
Fig. 12 Thickness of myelin sheath plotted against inner diameter of axons, measured in the superior longitudinal fascicle of the monkey. The correlation coefficient is 0.75; the average thickness of the myelin sheath is 0.09 μm, the median 0.08 μm
Fig. 12 Thickness of myelin sheath plotted against inner diameter of axons, measured in the superior longitudinal fascicle of the monkey. The correlation coefficient is 0.75; the average thickness of the myelin sheath is 0.09 μm, the median 0.08 μmCC BY · PubMed Central
Fig. 13 Largest axon found in our material (not contained in samples measured). It was located in the region of the superior longitudinal fascicle of human brain 2 (left hemisphere). Bar 5μm
Fig. 13 Largest axon found in our material (not contained in samples measured). It was located in the region of the superior longitudinal fascicle of human brain 2 (left hemisphere). Bar 5μmCC BY · PubMed Central

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Citations

Cites

Show all 98 references

Research works printed but not linked: 5

  1. Aboitiz F, Ide A, Olivares R (2003) Corpus callosum morphology in relation to cerebral asymmetries in the postmortem human. In: Zaidel E, Iacoboni M (eds) The parallel brain: the cognitive neuroscience of the corpus callosum. MIT Press, Cambridge, pp 33–46
  2. Allman J (1999) Evolving brains. Scientific American Library, New York
  3. Bürgel U (1999) Kartierung langer Faserbahnen im adulten menschlichen Gehirn. Geschlechtsunterschiede, Lateralisation und Variabilität. Dissertation at the Faculty of Medicine, Heinrich-Heine-Universität Düsseldorf
  4. Häggqvist G (1936) Analyse der Faserverteilung in einem Rückenmarkquerschnitt (Th 3). Z Mikrosk Anat Forsch 39:1–34
  5. Palay LS, Chan-Palay V (1974) Cereb Cortex. Springer, Berlin

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Metadata

Authors
Liewald, D., Miller, R., Logothetis, N., Wagner, H.-J., & Schüz, A.
Affiliations
  • Max Planck Institute for Biological Cybernetics (DE)
  • University of Otago (NZ)
  • University of Tübingen (DE)
Corresponding author
Schüz, Almut
ORCID
Venue
Biological Cybernetics
Publisher
Springer Science and Business Media LLC
Published
2014-08-21
Volume
108
Issue
5
Pages
541-557
ISSN
  • 0340-1200 (ISSN-L)
  • 1432-0770
DOI
10.1007/s00422-014-0626-2
PMC
PMC4228120
OpenAlex
W2046529900
Cited by
322
References
98
Citations by year
2026: 16 · 2025: 28 · 2024: 25 · 2023: 36 · 2022: 39 · 2021: 37 · 2020: 39 · 2019: 35 · 2018: 28 · 2017: 14 · 2016: 21 · 2015: 4
FWCI
10.17
Type
journal article
Language
en
Open access
Licence
Locations
  • Biological Cybernetics (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • MPG.PuRe (Max Planck Society) (submittedVersion, other-oa)
  • Max Planck Digital Library (submittedVersion)
Topics
  • Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Advanced Neuroimaging Techniques and Applications
  • Health Sciences › Medicine › Anatomy › Classical Anatomy and Histology
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Visual perception and processing mechanisms
Keywords
axon diameter, cortical white matter, superior longitudinal fasciculus, corpus callosum, myelinated axons, myelin thickness, hemispheric lateralization, human brain, macaque brain, conduction velocity, diffusion-weighted imaging
MeSH terms
Aged, Aged, 80 and over, Animals, Axons, Cerebral Cortex, Humans, Functional Laterality, Macaca mulatta, Male, Myelin Sheath, Electron Microscope Tomography, White Matter

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